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Authors:
Jaakko Leppänen, Susanna Siitonen and Jan Weckström
Title:
The stability of Cladoceran communities in sub-Arctic NW Finnish Lapland lakes
The affiliations and addresses of the authors:
Corresponding author:
Jaakko Leppänen
Department of Environmental Sciences
P.O. Box 65, FIN-00014, University of Helsinki, Finland
+358415439736
Susanna Siitonen
Department of Environmental Sciences
P.O. Box 65, FIN-00014, University of Helsinki, Finland
Jan Weckström
Department of Environmental Sciences
P.O. Box 65, FIN-00014, University of Helsinki, Finland
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Abstract
It is difficult to plan restoration projects or study the amount of disturbance in aquatic ecosystems if
background conditions are not known. Zooplankton, especially cladocerans (water fleas), has
proven highly useful as a reliable indicator of environmental change. Cladocerans preserve well in
sediments and thus allow for the analysis of historical communities. To assess the stability of
cladoceran communities in lakes with low human impact, we compared pre-industrial and modern
cladoceran assemblages (top-bottom analysis) in 32 sub-Arctic lakes in NW Finnish Lapland. We
used a data set of measured environmental variables to determine their explanatory power on
cladoceran assemblages. While cladoceran assemblages at the community level have remained
relatively stable between the pre-industrial and modern samples, a clear change at the genus level
was observed with a significant proportional increase in Bosmina (Eubosmina) spp. (Wilcoxon
signed rank test z = 2.75 p = 0.006). The amount of organic matter in the sediment (measured as
loss on ignition (LOI)) explained the largest proportion of the variation in the cladoceran
community. Since LOI is strongly correlated to climatic factors, the increased abundance of B.
(Eubosmina) spp. may ultimately be related to climate warming. As the top-bottom approach is
comprised of two temporal snapshots, it cannot provide the exact time of community change. This
shortcoming is of special importance for restoration and management planning.
Keywords: Cladocera, community change, palaeolimnology, climate change, reference conditions,
Finland
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Introduction
There is a long tradition of using (sub)fossil species assemblages to investigate the effects of both
natural and human-induced environmental disturbances. Zooplankton are known to respond
strongly to environmental changes (Jeppesen et al. 2011) and some groups even have potential to be
used as early warning organisms regarding ecosystem changes (Pace et al. 2013). Further,
zooplankton plays a key role in many restoration projects where the goal is to halt or reverse lake
eutrophication (Gulati et al. 2008), making it an important group for efforts which aim to improve
the quality of inland waters. In fact, Luoto et al. (2013) developed a cladoceran (Branchiopoda:
Phyllopoda) -based model, which can be used to estimate the ecological status of a given water
body and to define reference conditions. Also, cladocerans have been used to evaluate the success
of restoration projects in cases, where historical cladoceran community data have been available
(e.g. Louette et al. 2009). However, almost all surface waters in Europe have already changed
during the last centuries due to land use, contamination and climate change (Wetzel 1992; Bennion
and Batterbee 2007), but monitoring programs extending over decades are very rare. It is therefore
difficult to assess or to predict the effects of any disturbance or to succeed in restoration projects if
the environmental history or ongoing ecological trends are not assessed. Lake sediments have the
potential to store an enormous amount of environmental information and the palaeolimnological
approach can be used as a tool to uncover the historical conditions of past aquatic environments
(Smol 1992; European Union 2000). Cladocerans are regarded as one of the most useful
palaeolimnological tools to track environmental change (Eggermont and Martens 2011). Cladoceran
subfossils in families Chydoridae and Bosminidae preserve well in sediments and can be identified
in some cases to species group level (Frey 1987). Cladocerans have been used in
palaeolimnological research for more than 50 years with methods varying from simple descriptive
studies (Frey 1962) to computer-powered ecosystem modelling of historical environments (e.g.
Korhola et al. 2002). Cladoceran-based palaeolimnological studies include climate change research
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(Lotter et al. 1997; Korhola 1999; Sarmaja−Korjonen et al. 2006), calcium decline research
(Jeziorski et al. 2008), reconstruction of water level fluctuations (Sarmaja−Korjonen and Alhonen
1999; Korhola et al. 2000; Siitonen et al. 2011), food web studies (Rawcliffe et al. 2010), and
reconstruction of trophic state (Korponai et al. 2011).
Lakes and rivers in NW Finnish Lapland are regarded as among the most pristine environments in
the world (Hettelingh et al. 1992; Rühling and Steinnes 2002). Because the level of anthropogenic
disturbance is extremely low, these ecosystems provide excellent opportunities to study baseline
conditions and the long-term stability of biological communities by using palaeolimnological
methods. Usually the fossil biota assemblages from a whole sediment sequence is studied to assess
possible past environmental trends (e.g. Manca et al. 2007), but when studying a large number of
lakes, the so called top-bottom or “before-after” approach is perhaps the most useful option
(Michelutti et al. 2001; Weckström et al. 2003). The topmost centimetre of lake sediment represents
the modern environmental conditions, whereas the “bottom” sample reflects a point of time in the
past, e.g. pre-industrial conditions. The top-bottom approach thus enables the assessment of system
stability on a regional scale. It should be noted, however, that this approach has a notable
shortcoming as it provides information of only two single periods of time, lacking the possibility to
track short-lived fluctuations between the two periods of interest.
In this study, we used a top-bottom data set consisting of 32 sub-Arctic lakes to 1) explore which
environmental factors exert the strongest impact on the cladoceran community structure, and 2) to
compare the species composition between the pre-industrial and modern samples in NW Finnish
Lapland. We aim to provide new information about the applicability of reference condition analysis
based on one temporal snapshot (the bottom sample) in some of the least disturbed regions in the
world. Further, our study intends to add new insights to the discussion regarding the stability of
zooplankton communities and environmental change during the last few centuries in NW Finnish
Lapland.
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Materials and methods
Study area
The 32 lakes are situated in sub-Arctic NW Finnish Lapland, (except for one site located in
Norway), an area with a notable eco-climatic gradient (Fig. 1). The lakes span from the boreal
forest to the mountain birch woodland and further across the tree line to the tundra. The study lakes
are generally small (0.9–115 ha, mean 15 ha) and shallow (1-25 m, mean 6 m), they are relatively
neutral (pH ranges within 4.9–7.6, mean 6.6) and have low conductivity (0.4–5.1 mS/cm, mean 2.1
mS/cm). Total phosphorus (TP) varies between 1.5-46 µg/L (median 5 µg/L) and total nitrogen
(TN) between 54-1,500 µg/L (median 280 µg/L) (Table 1; Online Resource 1). According to the
dataset retrieved from the KNMI Climate Explorer (van Oldenborgh 1999) online data bank
(http://climexp.knmi.nl/), the annual mean temperatures (averages 1961-2011) in the study area
range from -1.2 ˚C in the south to -2.1 ˚C in the north. This is also reflected in the annual ice cover
period of the lakes varying from ca. 200 days in the south to 260 days in the north (Weckström et al.
2014). The study area is relatively pristine as it lacks big population centres, heavy industry, and the
effects of atmospheric transportation of pollutants are generally negligible (Paatero et al. 2008). The
air quality is considered as one of the cleanest in Europe (Hettelingh et al. 1992; Anttila et al. 2011).
According to weather data provided by the KNMI database, the annual temperature averages and
average daily precipitation have increased during the past decades in the study area (Fig. 1). Recent
climate change can thus be considered as the only regional environmental variable that has had an
impact on all study lakes during the past decades.
Fish populations
The important role of fish as a determinant of the cladoceran community structure has been shown
in many studies (e.g. Hrbacek et al. 1961; Brooks and Dodson 1965; Persson 1986), but in this
study it is assessed only at a general level because no exact data of possible fish introductions and
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their timing are available. Most of our study lakes are either naturally inhabited by fish, or have
been stocked, and according to Tammi et al. (2003), the number of fish species in these lakes is
mostly between 1 and 3. However, the shallow (water depth < 1.5 m) and remote high altitude
hilltop lakes are most likely fishless. In our study lakes the most common fish species are whitefish
(Coregonus lavaretus), arctic char (Salvelinus alpinus), brown trout (Salmo trutta), and also perch
(Perca fluviatilis) especially in the forested catchments. Brown trout and arctic char are the most
common species able to inhabit the high altitude and cold tundra lakes, whereas whitefish is
generally restricted to lower altitude warmer water lakes (Tammi et al. 2003). Whitefish is probably
the most intensively introduced fish species in northern Finland (Tammi et al. 2003). However,
there are no reliable registers or data regarding the time, place and magnitude of fish introductions
available.
Sampling
Water samples were retrieved from 1 meter depth using a limnos sampler and geographical
characteristics were determined using topographic maps. The water samples (500 ml) were
collected in acid-washed polyethylene bottles and stored at 4 ºC for chemical analyses. Water
chemistry analyses were carried out using standard methods. For more information, see Weckström
et al. (1997) and Weckström and Korhola (2001).
Three parallel surface sediment cores were retrieved with a Limnos-type gravity corer from the
deepest part of each lake in autumn 2008. Sediment cores were combined in order to get enough
material for analyses and subsampled into 1 cm thick sequences, packed in small plastic bags and
stored in 4°C cold storage. Surface sediment samples (0-1 cm) are thought to represent the present,
and the 1 cm sediment slices from varying depths between 4 and 15 cm represent the pre-industrial
era. The retrieval depths of bottom samples were determined in the field and the assessment was
based on known sedimentation rates, local characteristics and visible sediment properties. In
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general, at high altitude tundra lakes, the bottom sample was taken from an average depth of 9 cm,
whereas at lakes located in mountain birch vegetated catchment area, the bottom sample was taken
from an average depth of 13 cm. At lakes located in coniferous forest catchments, the bottom
sample was taken from an average depth of 14 cm. Sedimentation rates of these sub-Arctic lakes are
generally low and are well known in the region (e.g. Korhola and Weckström 2004; Siitonen 2005;
Weckström et al. 2014). The laboratory procedure and the identification of cladoceran is based on
Szeroczyńska and Sarmaja−Korjonen (2007). Cladoceran taxonomy is currently under a thorough
revision. In this study, the nomenclature is based on Szeroczyńska and Sarmaja−Korjonen (2007),
Van Damme and Dumont (2008), Sinev (2009), Korovchinsky (2016), and Sinev and Dumont
(2016). The sediment samples were prepared by heating and stirring 1 – 2 cm3 of sediment in 10%
KOH for 30 min and sieving through a 50 µm mesh with tap water. Cladoceran remains were
identified from permanent slides under a light microscope using 100-400 x magnification. The
counted number of individuals is based on the most common fragment of each species. The results
are expressed as relative abundances.
Data analysis
It has recently been proposed that a minimum number of 70-100 individuals should be counted
when studying claodoceran subfossils (Kurek et al. 2010). Here, at least 75 individuals per sample
were counted. The possible bias in species richness resulting from different total counts per sample
was corrected using rarefaction analysis (Birks and Line 1992). We used a Simple Mantel’s test
(Mantel 1967), which is a non-parametric test for correlation of two matrices, to study whether
environmentally similar lakes also have similar cladoceran communities. The Simple Mantel’s test
was applied to environmental factors (euclidean distance matrix) and cladoceran species
composition (Bray-Curtis dissimilarity matrix). Environmental data were Z-standardised and
cladoceran community data were square root-transformed prior to matrix calculations. Due to the
short gradient length of species compositional turnover along the first DCA axes (1.9 SD units), the
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relationships between environmental variables and modern cladoceran assemblages were studied
using redundancy analysis (RDA). In RDA, the pre-industrial samples were treated as
supplementary variables. Skewed environmental data were log10(x+1) -transformed prior to
analysis. To reduce multicollinearity, variance inflation factors (VIFs < 20) were used to select the
final set of environmental variables. However, also the known ecological importance or
combination of the environmental variables was taken into account. A similarity matrix was
constructed using the Bray-Curtis similarity index (Bray and Curtis 1957), which was calculated
from square root-transformed species abundance data. The matrix was used to detect significant
differences between pre-industrial and modern cladoceran communities by the analysis of similarity
(ANOSIM) method. ANOSIM is a non-parametric test of significant difference between two groups
(Clarke 1993). The similarity matrix was further used to quantify compositional differences for each
lake between the pre-industrial and the modern period. For individual lake comparisons, the Bray-
Curtis dissimilarity index was used, where the value of 0 resembles identical cladoceran
communities. The Wilcoxon signed-rank test (Wilcoxon 1945) was conducted to determine if
species proportional abundances had changed significantly since the pre-industrial era. The
Wilcoxon signed-rank test is a nonparametric test analogous to the dependent t-test. RDA was
performed using CANOCO for Windows 5.01 (ter Braak and Šmilauer 1997-2012), ANOSIM,
Mantel’s test and the rarefication analyses were conducted using the PAST statistics 3.1. software
(Hammer et al. 2001) and the Wilcoxon signed-rank test was performed using the IBM SPSS
Statistics 22 software (IBM Corp 2013). To analyse the general environmental preferences of
cladoceran taxa, the study lakes were grouped into three catchment categories based on the
prevailing ecotone of the catchment area (coniferous forest, mountain birch woodland, and barren
tundra). These catchment categories consisted of 17, 7, and 8 lakes, respectively.
Results
Modern and pre-industrial cladoceran communities in NW Finnish Lapland
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Fossil cladoceran remains were generally well preserved in the sediment samples. Out of 36 taxa
identified, Chydorus spp. and Bosmina (Eubosmina) spp. were most widely distributed and were
detected in all lakes both in pre-industrial and in modern samples. Bosmina (Eubosmina) spp. was
proportionally most abundant in 20 lakes in modern samples (average 37.6% SD ± 18.1 %) and in
16 lakes in pre-industrial samples (30.6 % SD ± 16.9 %). In modern samples, a total of 13
cladoceran taxa were present in all catchment vegetation types (Table 2). The rarefaction-corrected
number of taxa varied from 19 (lake 8) to 7 (lakes 12 and 49) in modern samples and from 18 (lake
9) to 6 (lake 6) in pre-industrial samples (Fig. 4).
Environmental variables and cladoceran assemblages
The Simple Mantel’s test exhibited positive (R = 0.40) and significant (p = 0.003) correlation
between similarity matrices of cladoceran communities and environmental factors. After screening
the original 31 environmental variables (Table 1; Online Resource 1) by VIF only 10 environmental
variables (mire area, LOI, sample depth, air temperature, pH, conductivity, calcium, total organic
carbon (TOC), total P, and total N) were included in RDA. These 10 environmental variables
explained 83.5% of the explanatory power of the 31 original environmental variables. After
variance partitioning, LOI was identified as the environmental variable explaining the largest part of
the variation in the cladoceran populations in our data set (Table 3). The correlation structure of
cladoceran populations and environmental variables is presented as an RDA biplot (Fig. 2). There,
the barren tundra lakes are plotted together indicating lower LOI, TOC, temperature and nutrients
values when compared to catchments with prevalent tree vegetation. According to RDA, no
common characteristics can be seen between the pre-industrial and modern samples (Fig. 3).
Cladoceran community changes since pre-industrial era
When all lakes were treated as one group, no significant differences were observed between pre-
industrial and modern cladoceran communities (ANOSIM R = -0.0066, p = 0.59). Results obtained
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by similarity matrix analysis demonstrated that the average dissimilarity value between pre-
industrial and modern samples, when lakes were treated individually, was 0.29 SD ± 0.12. The
maximum dissimilarity value was 0.64 (Lake 62) and the minimum 0.13 (Lake 18). The largest
positive change in the rarefied species number between the pre-industrial and modern sample was in
lake 8, where the number of taxa increased by four. The largest negative change was recorded in
lake 26, where the number of taxa decreased by five (Fig. 4). The planktonic Bosmina (Eubosmina)
spp. increased significantly since the pre-industrial period (Wilcoxon signed rank test z = 2.7 p =
0.006), while changes concerning other species were not statistically significant. The proportion of
Bosmina (Eubosmina) spp. increased in 22 lakes by an average of 14.9 % and decreased in 10 lakes
by an average of -8.9 %. Further, the grouping of all identified planktonic taxa (Bosmina
(Eubosmina) spp., Polyphemus pediculus, Daphnia spp.) together, revealed a proportional increase
in 23 lakes by an average of 14.1 % and a decrease in nine lakes by an average of -8.9 %. The
change considering all planktonic species was significant (Wilcoxon signed rank test z = 2.8 p =
0.004). When lakes were grouped according to their catchment type (tundra, mountain birch,
confierous forest), the changes in community and species level were not significant.
Discussion
Environmental variables and cladoceran assemblages
Only Bosmina (Eubosmina) spp. and Chydorus spp. were found in all studied lakes. They are both
common in Northern Scandinavia (Korhola 1999; Rautio 2001; Brancelj et al. 2009). The overall
composition of cladoceran assemblages found in NW Lapland resembles those of the Central
Canadian treeline region (Sweetman et al. 2008) and Nova Scotia, Canada (Korosi and Smol 2011).
The clear correlation (Simple Mantel’s test R = 0.4, p = 0.003) regarding the degree of dissimilarity
between cladoceran communities and environmental parameters suggests that environmental factors
contribute strongly to species assemblages in our study lakes. Among the environmental variables
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studied, only LOI explained a statistically significant portion of the variation in the species data.
LOI values provide a crude measure of the organic carbon content in sediments thus reflecting
primary production, catchment type and decomposition speed in the environment. Tundra lakes are
generally characterized by low LOI, TOC, temperature and nutrient concentrations (Fig. 2)
(Korhola and Weckström 2004). It has been suggested that fluctuations in LOI are connected to
changes in air temperature (Willemse and Törnquist 1999; Battarbee et al. 2001; Nesje and Dahl
2001; Kaplan et al. 2002). The correlation between climatic variables and LOI is also visible in this
data set (Table 1), where the role of eco-climatic gradients is clearly visible. High altitude and
latitude lakes, which are usually cool with low nutrient and low TOC concentrations, are
characterized by low LOI values, when compared to low altitude forest lakes. The fact that 17 taxa
were absent from tundra lakes, also reflects the effect of altitude and characteristics related to
altitude on the cladoceran species composition.
It is most likely that fish have some impact on cladoceran communities in our study lakes, although
our data do not clearly support this. Whitefish, especially the densely raked form (C. lavaretus
pallasi), feeds almost exclusively on zooplankton during all its life (e.g. Säisä et al. 2008), and may
thus have a high and direct impact on cladoceran communities. In contrast, as arctic char and brown
trout prefer larger prey items, such as invertebrates like gammarids and copepods (Crustacea), they
have an indirect impact on cladocerans by decreasing the pressure of invertebrate predation on
cladocerans (e.g. Seppovaara 1969; Milardi et al. 2016). However, in this study the impact of fish
on cladoceran communities cannot be quantified because no data on the dynamics of fish
populations are available. Moreover, because the dominant cladoceran species Bosmina
(Eubosmina) spp. is known to thrive in lakes with versatile fish communities (Tolonen 1997;
Amsinc et al. 2006), any generalizations regarding the effects of fish are very difficult.
In contrast, our results, concerning the role of primary production and climate-related
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environmental variables on cladoceran species composition, are in good accordance with other
circumpolar studies (e.g. Korhola 1999; Brancelj et al. 2009; Sweetman et al. 2010; Korosi and
Smol 2011; Luoto et al. 2013). These studies indicate that nutrients, dissolved organic carbon and
lake water temperature are important variables controlling cladoceran community structure in
Canadian treeline region (Sweetman et al. 2010), lake depth and dissolved organic carbon in Nova
Scotia, Canada (Korosi and Smol 2011), lake depth, sediment organic content, epilimnetic summer
temperature, lake perimeter and lake catchment area in Finnish Lapland (Korhola 1999), and total
phosphorus in Finland (Luoto et al. 2013). In a study of 294 remote cold water lakes across Europe,
altitude was found to be the most important variable affecting the cladoceran community structure
(Brancelj et al. 2009).
Changes in cladoceran assemblages since the pre-industrial period
The lack of community level change between pre-industrial and modern samples suggests that
cladoceran communities have remained relatively stable during the recent centuries. Still, the
stability varied between lakes, and few lakes exhibited relatively high dissimilarities between pre-
industrial and modern samples (e.g. lakes 62 and 7). The most striking feature in our study lakes is
the increased relative abundance of planktonic Bosmina (Eubosmina) spp. in 22 out of 32 lakes,
whereas the corresponding decline in other taxa is highly variable. The reasons behind this shift are
most probably either changes in fish populations or climate warming. Fish may have high-
magnitude impacts on zooplankton communities (e.g. Brooks and Dodson 1965) and this has also
previously been detected in sub-Arctic lakes (Bøhn and Amundsen 1998; Donald et al. 2001;
Milardi et al. 2016). However, reliable historical records are not available and current fish data
concerning the study lakes are scarce. Planktivorous fish have been noted to prefer larger
cladoceran taxa, resulting in an overall decrease in the size structure of cladoceran communities e.g.
the shift from larger Eubosmina spp. to small Bosmina species (e.g. Stenson 1976). Such a shift,
however, is not detectable in our study lakes. The impact of predator fish on cladocerans is usually
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not direct, but a result of trophic cascades (Brooks and Dodson 1965; Hall et al. 1976). The changes
in intensity of invertebrate predation can be detected as morphological changes in Bosmina
longirostris, but the applicability of Bosmina (Eubosmina) spp. in predation assessments is poor due
to contrasting results in literature (e.g. Sprules et al. 1984; Johnsen and Raddum 1987). In the
absence of species data of invertebrate predators, it is not possible to provide any information on
this issue. However, the minor changes in the cladoceran communities in most of our study lakes
since the pre-industrial time suggests that large-scale changes in fish population dynamics are not
likely.
The proportional increase in planktonic cladocera in the majority of the studied lakes is a significant
change that has occurred in the NW Finnish Lapland tree line region lakes during the last few
centuries indicating a presence of a regional baseline shift. The increasing abundance of planktonic
species, particularly Bosmina (Eubosmina) spp. in a relatively large geographical area suggest that
the shift may be a result of global climate change, which is reflected in NW Finnish Lapland as
increased temperatures and precipitation (Fig. 1). However, whereas lake surface water
temperatures in northern latitudes are increasing, the regional variation in warming trends suggests
that the connection between air and water temperatures is affected by local characteristics (O'Reilly
et al. 2015). Also, the climatic factors usually affect lake biota indirectly and the final impact
depends on lake and catchment characteristics of an individual lake (e.g. Battarbee 2000). The fact
that our study lakes may have responded to an increase in air temperatures and precipitation in a
number of ways, is also visible in our results (Fig. 3), where sample pairs do not exhibit any
common trends in relation to each other or to environmental variables. This may be the reason for
the low unique contributions of climatic factors showed in Table 3. However, some indications of
the impact of climate change on planktonic cladocerans can be seen. An increase in primary
production during the 20th century has already been recorded in Arctic lakes (Smol et al. 2005;
Michelutti et al. 2005). Further, the increase in planktonic diatom species since pre-industrial times
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has been detected in the Canadian treeline region (Rühland et al. 2003) and in Finnish Lapland
(Sorvari and Korhola 1998; Korhola et al. 2002; Sorvari et al. 2002). Shifts in diatom communities
in the sub-Arctic region have been linked to shortening of the ice-cover period, more stable
stratification and a longer growing season due to climate warming (Smol et al. 2005). Planktonic
cladoceran species may have benefited from this elevated food availability. In addition to these
already observed changes related to primary production of lakes, there are further and potentially
important connections between climate change, primary production and cladoceran communities.
Higher temperatures may have enhanced the growth of edible bacteria near the surface (Simon and
Wünch 1998) and increased precipitation may have accelerated the flush of allochthonous carbon
into the lakes, which is an important component of winter food for cladocerans in Finnish Lapland
(Rautio et al. 2011). Bosmina (Eubosmina) spp. may adapt to changes in food availability easier
than some other cladoceran species, since it has a versatile feeding mechanism, which enables it to
feed both on large (Johnsen and Borsheim 1988) and small (Borsheim and Anderssen 1987) food
particles. In stratified lakes the increased production may also enhance oxygen depletion in the
hypolimnion, especially in high latitude lakes with prolonged ice cover. This, in turn, may suppress
the occurrence of benthic species and increases the proportion of planktonic cladoceran taxa (e.g.
Nevalainen and Luoto 2012). However, data regarding oxygen dynamics in our study lakes are not
available.
Our results are similar to Jeziorski et al. (2015), who compared pre-industrial and modern
cladoceran assemblages in 60 lakes of far north Ontario, Canada. They recorded a significant
proportional increase in pelagic cladoceran species. Also Desellas et al. (2011) detected an increase
in the relative abundance of pelagic cladoceran species since pre-industrial times in 42 lakes in
Ontario, Canada. Korosi and Smol (2012) compared modern cladoceran assemblages with pre-
industrial assemblages in Nova Scotia, Canada. They showed a proportional, but non-significant
increase of Bosmina (Eubosmina) spp. in 32 out of 48 lakes. However, Sweetman et al. (2008)
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argued that cladoceran assemblages have not experienced any directional changes since pre-
industrial times in 50 tree-line region lakes in the central Canadian Arctic, despite a significant shift
towards planktonic species in the diatom communities. Although the top-bottom approach is highly
useful when assessing if changes in lake ecosystems have occurred since pre-industrial times on a
regional scale (a large number of lakes), it does not allow for pinpointing exactly when the
change(s) have occurred (Bennion et al. 2011). Especially for lake management purposes, a set of
chronological snapshots from the sediment sequences are needed. This is particularly important
when changes are rapid (e.g. due to pollution accidents), as it is impossible to detect any baseline
shifts prior to the accident without an adequate chronology of conditions.
In 10 out of 32 lakes the proportion of Bosmina (Eubosmina) spp. decreased. This opposite genus
level change may be caused by local environmental factors, which could have suppressed the
impact of regional stressors as suggested by Alric et al. (2013). Forestry (Bredesen et al. 2002),
fishing or fish introductions (Donald et al. 2001; Milardi et al. 2016) and reindeer herding
(Kuzmina and Leshko 2002) are likely the most important local human-induced factors that may
have had direct or indirect effects on cladoceran populations in our study lakes. The lakes
displaying a decreased proportion of Bosmina (Eubosmina) spp. are relatively shallow and represent
a wide spectrum of catchment variables. The average depth of these lakes was 4.5 m, while the
average depth of the other lakes was 8.7 m. In general, shallow lakes are more vulnerable to
environmental changes compared to deep lakes due to lower heat capacity (Shutner et al. 1983),
lower dilution capacity (Janse et al. 2008) and less diverse fish communities (Eloranta et al. 2015).
Conclusions
Cladoceran assemblages in NW Finnish Lapland have remained relatively stable during the last
centuries, however, some changes could be observed. The increased abundance of Bosmina
(Eubosmina) spp. in many of the lakes can be regarded as a baseline shift due to current climate
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change. In contrast, some of the study lakes exhibited a decreased abundance of Bosmina
(Eubosmina) spp., which is likely related to local, catchment-related stressors. The top-bottom
approach is a powerful tool when a large number of sites are studied. However, in order to assess
the exact time, magnitude and speed of change(s) or baseline shift(s), either continuous sediment
series or a series of snapshots should be used instead. The recognition of directional changes and
the obtained set of multiple reconstructed past time slices may greatly assist in the planning of
restoration procedures.
Acknowledgements
This work was funded by Tellervo and Jussi Walden foundation. We thank Sanna Korkonen and
Juha Niemistö for help in the field.
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Tables
Table 1 Summary of environmental variables of the studied lakes. Coordinates are in WGS84 coordinate system, Area
= lake area, LOI = loss on ignition, depth = maximum water depth, Airtemp = average July air temperature, Ptot = total
phosphorus and Ntot = total nitrogen in water samples. Lakes are presented in ascending altitudinal order. A more
comprehensive list of environmental variables (including lake perimeter, catchment area, distance to tree line,
alkalinity, concentrations of K, Ca, Na, Mg, TOC, NH4-N, PO4-P, Cl, NO23N, SiO2, turbidity, SO4 and CNR) is
available as supplementary data (Online Resource 1)
LakeLatitude
(N)Longitude
(E)Altitude (m.a.s.l)
Area (ha)
LOI (%)
Depth (m)
Airtemp (°C)
pHConductivity (mS/cm-1)
Ptot (µg/L-1)
Ntot
(µg/L-1)
25 69.070 20.880 930.9 1.69 41.4 3.35 8.50 6.24 0.60 4.00 120.00
62 69.240 21.507 897.0 6.03 24.8 9.50 8.60 6.93 2.60 1.50 69.00
58 69.266 21.189 895.0 1.15 14.16 3.50 9.60 6.99 1.80 4.00 110.00
54 69.030 21.125 796.4 9.33 33.6 8.00 9.20 6.80 1.40 1.50 110.00
49 69.080 20.670 776.3 16.10 16.9 12.10 9.40 6.69 0.90 1.50 54.00
55 69.056 21.047 774.0 20.44 34.04 2.00 9.30 6.98 2.00 1.50 140.00
63 69.191 21.454 704.3 100.35 14.3 21.50 9.70 7.59 4.70 4.00 77.00
18 68.920 20.970 526.0 3.85 55.0 1.45 10.80 7.13 3.40 5.00 270.00
48 68.700 21.500 487.9 28.04 35.1 12.60 11.20 7.09 2.30 5.00 150.00
21 68.700 21.480 480.6 18.01 28.1 25.00 11.30 7.15 3.40 1.50 130.00
17 68.900 21.070 463.0 6.05 48.3 1.70 11.30 6.90 2.50 3.00 240.00
20 68.850 21.200 449.1 115.18 28.7 5.15 11.30 6.98 2.40 1.50 200.00
26 69.180 20.720 355.0 7.21 59.6 3.40 11.10 6.97 3.40 4.00 290.00
15 68.480 22.170 346.0 12.89 68.1 1.75 12.20 7.12 2.90 1.50 360.00
31 68.470 22.970 344.0 2.22 63.0 5.30 12.30 7.06 3.00 4.00 230.00
27
604
605
606
607
608
609
610611612613614615
12 68.420 22.580 332.0 1.97 80.8 1.85 12.40 4.89 3.40 7.00 390.00
34 68.470 22.470 329.1 11.76 47.9 4.05 12.30 7.06 2.30 8.00 330.00
13 68.470 22.430 322.0 2.55 60.4 4.00 12.50 6.49 1.00 6.00 320.00
32 68.420 22.900 319.0 28.18 42.3 6.00 12.60 7.05 3.20 12.00 320.00
10 68.400 22.880 317.0 2.58 49.4 6.30 12.60 6.21 0.40 6.00 200.00
11 68.400 22.850 313.0 2.18 58.6 4.10 12.60 6.82 1.10 7.00 360.00
8 68.300 23.220 294.0 33.99 37.3 6.95 12.80 6.76 1.80 14.00 330.00
9 68.330 22.950 290.0 2.62 63.6 1.75 12.10 6.60 1.80 46.00 560.00
3 67.850 24.180 268.0 7.14 64.1 4.00 13.30 6.19 1.10 7.00 330.00
7 68.200 23.180 263.0 0.90 61.2 4.40 13.00 6.55 1.20 9.00 390.00
4 67.980 23.680 262.0 10.67 71.8 3.30 13.10 5.29 0.70 1.50 330.00
28 67.880 23.870 254.0 18.80 35.7 1.45 13.30 6.92 3.00 25.00 480.00
30 68.130 23.370 253.0 1.33 83.6 4.30 13.20 5.69 0.50 12.00 640.00
6 68.120 23.370 252.0 1.52 88.0 4.30 13.10 5.29 0.50 8.00 460.00
5 68.010 23.400 249.0 4.34 50.1 3.35 13.20 6.76 2.10 38.00 1500.00
29 68.100 23.420 249.0 4.01 42.3 9.60 13.20 6.78 5.10 14.00 190.00
2 67.820 24.870 197.5 2.90 84.5 6.30 13.80 6.12 0.70 3.00 260.00
Mean
437.2 15.2 49.6 6.0 11.7 6.6 2.1 8.3 310.6
Table 2 Modern cladoceran taxa in lakes located in bare tundra, mountain birch woodland and coniferous forest –
vegetated catchment areas. The numbers preceding parentheses are average % of given species in all lakes situated in a
catchment vegetation type. Numbers within the parentheses indicate the number of lakes where the species was
detected. In the catchment vegetation type column the numbers indicate the total number of lakes in the ecotone
Barren
tundra (7)
Mountain
birch (8)
Coniferous
forest (17)
B. (Eubosmina) spp. 40.2 % (7) 39.9 % (8) 35.3 % (17)
Chydorus spp. 11.4 % (7) 4.0 % (8) 6.2 % (17)
Alonella nana 11.5 % (4) 17.1 % (8) 19.2 % (17)
Acroperus spp. 10.7 % (7) 3.1 % (7) 5.3 % (12)
28
616
617618619620
621
Alona affinis 0.1 % (1) 16.8 % (8) 16.7 % (17)
Eurycercus spp. 3.0 % (4) 4.5 % (8) 1.4 % (12)
Alonella excisa 1.6 % (3) 3.3 % (7) 1.1 % (9)
Alonopsis elongata 2.8 % (5) 0.8 % (5) 0.4 % (8)
Daphnia spp. 4.6 % (4) 0.6 % (3) 4.1 % (6)
Alona intermedia 2.3 % (5) 1.0 % (5) 0.4 % (8)
Ophryoxus gracilis 0.4 % (1) 1.2 % (4) 0.3 % (6)
Polyphemus pediculus 5.0 % (5) 3.0 % (8) 2.1 % (9)
Alona quadrangularis 3.0 % (2) 0.5 % (1) 0.8 % (5)
small Alona spp. 2.0 % (4) 0.7 % (3) 0.7 % (9)
Ceriodaphnia spp. 0.6 % (1) - 0.8 % (7)
Rhyncotalona falcata - 0.2 % (2) 0.1 % (2)
Flavalona rustica - 0.4 % (4) 0.9 % (7)
Sida crystallina - 0.4 % (4) 1.1 % (6)
Unapertura latens - 0.1 % (1) 0.2 % (4)
Camptocercus restricostris - 0.1 % (1) 0.1 % (2)
Graptoleberis testidunaria - 0.1 % (1) 0.4 % (4)
Coronatella rectangula - 0.1 % (1) 0.3 % (4)
Flavalona costata - 0.1 % (1) 0.1 % (1)
Alona guttata - 0.1 % (1) 0.1 % (2)
Paralona pigra - 0.1 % (1) 0.1 % (2)
Latona setifera - 0.1 % (1) 0.2 % (3)
Bythotrephes arcticus - 0.1 % (1) 0.1 % (1)
Ilyocryptus spp. - 0.1 % (1) -
Pleuroxus spp. - 0.1 % (1) -
Pleuroxus laevis - - 0.1 % (2)
Drepanothrix dentata - - 0.1 % (4)
Alonella exigua - - 0.1 % (1)
Number of taxa 15 28 30
Table 3 Summary of the results of variance partitioning for the screened 10 environmental variables
29
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623
Figure captions
Fig. 1 a Location of the study lakes and weather stations, lake altitudes, air temperatures, catchment
vegetation types and regional temperature and precipitation trends. Circles represent lake locations
and triangles represent the locations of the weather stations. b Lake altitude, average July air
temperature and catchment type (1 coniferous forest, 2 mountain birch and 3 bare tundra). Lakes are
ordered based on latitude (low latitude at the bottom) for easy interpretation of the ecoclimatic
gradient. c Average annual temperatures and average daily precipitation subtracted from 1959-2014
(Kilpisjärvi and Muonio) and 1961-2011 (Karesuando) average
Fig. 2 Redundancy analysis (RDA) correlation biplots for modern (s) and pre-industrial (b)
cladoceran samples and 10 pre-screened environmental variables. Open circles represent
catchments dominated by coniferous forest, grey circles represent catchments dominated by
mountain birch woodland, and closed circles represent barren tundra catchments
Fig. 3 Arrows indicating differences between pre-industrial and modern samples in a coniferous
forest catchment, b mountain birch catchment and c barren tundra catchment. The arrows point
30
Variance explained p= Covariation p= Unique
contribution Unexplained
Mire area 5.8 0.08 54 0.94 1 45LOI 20.1 0.001 48 0.002 7 45Sample Depth 14.0 0.001 51.4 0.11 3.6 45Air Temperature 10.8 0.001 52.3 0.28 2.7 45pH 11.2 0.003 52.1 0.23 2.9 45Conductivity 7.0 0.03 51.1 0.06 3.9 45Calsium 8.0 0.01 52.2 0.24 2.8 45TOC 14.2 0.003 51.3 0.08 3.7 45Ptot 3.4 0.36 53.4 0.67 1.6 45Ntot 6.8 0.04 51.4 0.11 3.6 45
624
625
626
627
628
629
630
631
632
633
634
635
636
637
638
639
640
641
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646
from the pre-industrial towards the present sample reflecting the calculated change in cladoceran
community as a function of time. The explanation power and direction of change of the
environmental variables used in the analysis are presented in figure 2
Fig. 4 Stratigraphic diagram of differences in abundance regarding the 10 most common cladoceran
species detected in pre-industrial and modern samples and modern lake catchment vegetation types
(coniferous forest 1, mountain birch 2 and barren tundra 3), species richness and dissimilarity
values. Faunal change is presented as % abundances. Lakes are in altitudinal order (lowest elevation
at the bottom)
Figures
31
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32
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